The study, published in the leading scientific journal Nature Plants, identified a gene that controls the availability of sugar to a growing seed shoot--especially when under flooded conditions.

"The seed of rice is unusual among crops because it can germinate and grow into a young plant that can capture light energy even when the entire process occurs underwater," said Julia Bailey-Serres, one of the paper's authors and a professor of genetics at UC Riverside. "The gene identified--the AG1 gene--helps in this process by allowing energy reserves that are in the seed to be efficiently moved to the growing shoot. The seed planted underwater grows into a seedling that can escape a shallow flood."

This process regulated by this new gene is opposite of that regulated by the SUB1A gene that was discovered previously to enable rice plants to survive complete submergence due to a seasonable flood. Bailey-Serres, who has worked extensively on the mechanism of submergence tolerance, commented, "Plants with SUB1A essentially hibernate when they are underwater; a situation where energy reserves are safeguarded."

A surprising find

AG1 creates an 'all or nothing' escape mechanism that tricks the seed into thinking that more sugar should be given to its shoot--the plant part that grows into stems and leaves--so that the seed underwater is able to more quickly grow and reach the surface of the water. The mechanism can work up to a water depth of 10 cm and can get 'activated' as soon as the seed is sown underwater.

"The gene that allows the seed to escape a flood, the AG1 gene, is one of a family of 13 genes in rice," explained Bailey-Serres, the director of UC Riverside's Center for Plant Cell Biology. "Other members of this family recently have been shown by a team of university researchers and a plant biotech group at Syngenta, to help the plant to move sugar from leaves to the young developing seed in fertilized flowers. When and where to move and use sugars is important. We think the important gene tells the cell that it does not have enough sugar--keeping the tap open for more to be moved from the seed to the growing shoot."

Surviving under water

Rice survival under flooding is also important when it comes to direct seeding, where seeds do not have to be pre-germinated and then transplanted. With direct seeding, seeds can be directly sown or broadcasted into the field, rather than painstakingly transplanted into the field. This is highly desired by rice farmers.

Moreover, one of the major limiting factors to direct seeding is weeds because these can germinate well under air--although not underwater without air--so if rice can germinate well underwater while none of the weeds do, then rice will be able to out-compete the weeds.

Mystery of the missing gene

"One thing that I've noticed is that the Indica varieties, which are the ones mostly grown in the tropical parts of Asia, are very much lacking in the trait or ability to grow under flooded conditions," said IRRI's Tobias Kretzschmar, the first author of the research paper. "But in Japonica, grown in the more temperate regions of Asia, Australia or the United States, the trait is present. That's why these varieties have fewer problems with direct seeding."

He explained that the missing trait is a problem, especially with modern Indica varieties as traditional ones have it, whereas modern ones do not.

Looking for an answer

"We looked at a third to a half of the IRRI released varieties, but the gene is missing," Kretzschmar said. "At first, we thought that maybe it was actively bred out, meaning that it has some negative effect so the IRRI breeders selected against it."

IRRI researcher Endang Septiningsih, who initiated and led the project, looked for a yield penalty or negative effect on the yield by AG1 but found none.

"We actually think it got lost," Kretzschmar said. "And we knew where it got lost. The gene got lost at the stage when IR8, the famous miracle rice variety, was bred because one of the parents had the gene, while the other did not."

Fitting pieces together

"I guess it was just never needed as a trait because almost every time the varieties were transplanted, there was no pressure for it," Kretzschmar explained. "If they had direct seeded then they probably would have retained that gene from the very beginning. But now that direct seeding is becoming popular, we've realized that we need that gene in the breeding program. So basically through the marker-assisted backcrossing approach, as it was done with the SUB1A gene introgression, which significantly reduces the breeding period, you can re-introduce the gene and then fix it within one and a half to two and a half years."

The way forward

With the unfolding of the 'AG1 secret' though, the research team's work is far from done.

"AG1 works well on moderate stress conditions. When we combined it with the SUB1A gene in the same genetic backgrounds it worked well, although they have opposing mechanisms. In severe stress conditions, however, AG1 alone is not sufficient--additional quantitative trait loci (QTLs) or genes that complement the AG1 mechanism will be needed. IRRI and partner universities are working hard in that direction," said Septiningsih, who recently joined the Department of Soil and Crop Sciences, Texas A&M University.

Another important question they are addressing is whether seed that can be directly seeded underwater - requiring the escape strategy - can also carry the SUB1A gene for submergence tolerance. This is a question that Bailey-Serres has been investigating with Septiningsih and Bangladeshi student Rejbana Alam, who contributed to the characterization of the role of AG1 during seed germination.

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Bailey-Serres received funding from the U.S. National Science Foundation for this project. Alam, the recipient of a Beachell Borlaug International Scholar Fellowship, is a graduate student working in her lab . IRRI was funded for this research by the German Federal Ministry of Economic Cooperation and Development, the Bill and Melinda Gates Foundation, and the Global Rice Research Partnership.

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